City's third defeat in quick succession and Stockport's first ever League win at Maine Road came courtesy of Nicky Weaver's wild dash from his goal and a Danny Granville's push on Alan Bailey in the ensuing chaos.
John Brandwood awarded the kick after consulting his assistant and Tony Dinning, threatened all night with an old-fashioned roasting by City's left-winger, Mark Kennedy, stepped up to have the last laugh from the penalty spot.
"I thought he was pushed, but I believe it might have been outside the area," said Stockport's delighted manager, Andy Kilner.
City should never have had to rely on such narrow margins. Playing with a surprising freedom and confidence after their defeat by Huddersfield and Wolves, they created an abundance of chances in the first-half, notably two headers from their new signings, Robert Taylor that went wide of the target, a lunging shot by Ian Bishop that hit the bar and one from Granville that shaved the post.
Stockport had shown enough on the break to suggest that they could pose problems of their own, but when City finally took the lead after 49 minutes it seemed that they were at last getting their promotion road show back on track.
Not surprisingly, the goal stemmed from a ball delivered by Kennedy, this time from a corner. Richard Jobson had the first attempt at forcing it in and his fellow defender, Gerard Wiekens, eventually fired it into the roof of the net.
Stockport's resilience was illustrated by the acrobatic save forced by Bailey immediately afterwards and, in the 65th minute, they were level. Dinning hit a post and Bailey, once a City apprentice, latched on to the rebound to slot it past Weaver.
The ebb and flow of a fascinating game continued with a sliced clearance that hit the Stockport woodwork, but it was the increasingly desperate search for a goal to restore their lead that left City fatally exposed at the back.
Their manager, Joe Royle, said Weaver had apologised for his blunder after the game. "He made a mistake but he's been magnificent and he'll still play for England," Royle said.
He remains philosophical about his side's faltering promotion campaign. "We're a point from the top half-way through the season and I would have settled for that," he said.
Blackburn Rovers (4-4-2): Kelly; Grayson, Peacock, Dailly, Harkness; McAteer, Frandsen, Carsley, Wilcox; Blake, Ward. Substitutes not used. Kenna, Ostenstad, Dunn, Taylor, Filan (gk).
Bolton Wanderers (4-4-2): Jaaskelainen; Phillips, Fish, Strong, Elliott (Holden, 79); Johansen (Hansen, 72), Jensen, Farrelly, Gardner; Taylor (Passi, 87), Gudjohnsen. Substitutes not used: Aljofree, Banks (gk).
Referee: D Pugh (Bebington).